Coevolutionary stability of host-symbiont systems with mixed-mode transmission.

The coevolution of hosts and symbionts based on virulence and mode of transmission is a complex and diverse biological phenomenon. We introduced a conceptual model to study the stable coexistence and coevolution of an obligate symbiont (mutualist or parasite) with mixed-mode transmission and its host. Using an age-structured Leslie model for the host, we demonstrated how the obligate symbiont could modify the host's life history traits (survival and fecundity) and the long-term growth rate of the infected lineage. When the symbiont is vertically transmitted, we found that the host and its symbiont could maximize the infected lineage's evolutionary success (multi-level selection). Our model showed that symbionts' effect on host longevity and reproduction might differ, even be opposing, and their net effect might often be counterintuitive. The evolutionary stability of the ecologically stable coexistence was analyzed in the framework of coevolutionary dynamics. Moreover, we found conditions for the ecological and evolutionary stability of the resident host-symbiont pair, which does not allow invasion by rare mutants (each mutant dies out by ecological selection). We concluded that, within the context of our simplified model conditions, a host-symbiont system with mixed-mode transmission is evolutionarily stable unconditionally only if the host can maximize the Malthusian parameters of the infected and non-infected lineages using the same strategy. Finally, we performed a game-theoretical analysis of our selection situation and compared two stability definitions.

Multivariate study of lice (Insecta: Psocodea: Phthiraptera) assemblages hosted by hummingbirds (Aves: Trochilidae).

Lice were collected from 579 hummingbirds, representing 49 species, in 19 locations in Brazil, Costa Rica, Honduras, Paraguay and Peru, at elevations 0­3000 m above sea level. The following variables were included in an ecological analysis (1) host species' mean body mass, sexual size dimorphism, sexual dichromatism, migratory behaviour and dominance behaviour; (2) mean elevation, mean and predictability of temperature, mean and predictability of precipitation of the host species' geographic area; (3) prevalence and mean abundance of species of lice as measures of infestation. Ordination methods were applied to evaluate data structure. Since the traits are expressed at different scales (nominal, interval and ratio), a principal component analysis based on d-correlations for the traits and a principal coordinates analysis based on the Gower index for species were applied. Lice or louse eggs were found on 80 (13.8%) birds of 22 species. A total of 267 lice of 4 genera, Trochiloecetes, Trochiliphagus, Myrsidea and Leremenopon, were collected, with a total mean intensity of 4.6. There were positive interactions between migration behaviour and infestation indices, with elevational migrants having a higher prevalence and abundance of lice than resident birds. Further, we found weak negative correlations between host body mass and infestation indices and positive correlations between mean elevation and prevalence and abundance of Trochiliphagus. Thus, formerly unknown differences in the ecological characteristics and infestation measures of Trochiliphagus and Trochiloecetes lice were revealed, which allows a better understanding of these associations and their potential impacts on hummingbirds.

Definitions of parasitism, considering its potentially opposing effects at different levels of hierarchical organization.

An annotated synthesis of textbook definitions of parasitism is presented. Most definitions declare parasitism is a long-lasting relationship between individuals of different species harming the hosts. The infection-induced costs are interpreted as diseases in the medical-veterinary literature. Alternatively, evolutionary ecologists interpret it as a reduction of host's fitness (longevity, fertility or both). Authors often assume that such effects decrease host population growth and select for antiparasitic defences, which is not necessarily true because infections may simultaneously express opposite effects at different levels of biological organization. (i) At the cellular level, infection-induced cell growth, longevity and multiplication may yield tumours maladaptive at higher levels. (ii) At the individual level, reduced host longevity, fertility or both are interpreted as disease symptoms or reduced fitness. (iii) Contrary to common sense, the growth rate of infected host lineages may increase in parallel with the individuals' reduced survival and fertility. This is because selection favours not only the production of more offspring but also their faster production. (iv) Finally, infections that reduce host individuals' or lineages' fitness may still increase infected host populations' growth rate in the context of ecological competition. Therefore, differences between parasitism and mutualism may depend on which level of organization one focuses on.

Relationship between body size and sexual size dimorphism in syringophilid quill mites.

A positive relationship of body size and sexual size dimorphism (males' size relative to females), called Rensch's rule, is often observed in comparisons within non-parasitic taxa. However, this allometric relationship has rarely been tested in comparisons across closely related parasite species. Since male sexual rivalry is often regarded as the main cause of this phenomenon, the present study tests this rule in a taxon where sexual selection is almost totally absent in males. Body size data of (non-physogastric) female and male quill mites (Acari: Syringophilidae) were gathered from the literature to investigate this relationship. The data set consisted of 113 species representing 8 genera. For the data set as a whole, increasing body size came together with decreasing relative body size of males (relative to females), a phenomenon known as converse Rensch's rule. Repeating the same analysis for the 8 genera separately, similar patterns were found in 4 significant and 3 non-significant cases. There was a significant tendency to comply with Rensch's rule only in one genus, the Neoaulonastus. Thus, converse Rensch's rule is the primary trend in syringophilid quill mites that appears repeatedly and independently in several genera. This phenomenon is probably caused by their extreme inbreeding, which strongly reduces sexual competition among males in this taxon.

A negative covariation between toxoplasmosis and CoVID-19 with alternative interpretations.

Coronaviruses may exert severely negative effects on the mortality and morbidity of birds and mammals including humans and domestic animals. Most recently CoVID-19 has killed about half million people (27th of June, 2020). Susceptibility to this disease appears to differ markedly across different societies but the factors underlying this variability are not known. Given that prevalence of toxoplasmosis in human societies may serve as a proxy for hygiene, and it also exerts both direct and immune-mediated antiviral effects, we hypothesize a negative covariation between toxoplasmosis and measures of the CoVID-19 pandemic across countries. We obtained aged-adjusted toxoplasmosis prevalence of pregnant women from the literature. Since the differences in the CoVID-19 morbidity and mortality may depend on the different timing of the epidemics in each country, we applied the date of first documented CoVID-19 in each country as a proxy of susceptibility, with a statistical control for population size effects. Using these two indices, we show a highly significant negative co-variation between the two pandemics across 86 countries. Then, considering that the wealth of nations often co-varies with the prevalence of diseases, we introduced GDP per capita into our model. The prevalence of toxoplasmosis co-varies negatively, while the date of first CoVID-19 co-varies positively with GDP per capita across countries. Further, to control for the strong spatial autocorrelation among countries, we carried out a Spatial Structure Analyses of the relationships between the date of first CoVID-19, prevalence of toxoplasmosis, and GDP per capita. Results of this analysis did not confirm a direct causal relationship between toxoplasmosis and susceptibility to the CoVID-19 pandemics. As far as an analysis of observational data let us to suggest, it appears that the interaction between CoVID-19 and toxoplasmosis is mediated by GDP per capita and spatial effects. This prompts the question whether the formerly known covariations of CoVID-19 and BCG vaccination or air pollution might have also emerged as spurious indirect effects.

Sex interacts with age-dependent change in the abundance of lice-infesting Amur Falcons (Falco amurensis).

Sex-biassed and age-biassed parasite infections are common in nature, including ectoparasites-vertebrate host systems. We investigated the effect of Amur Falcons' sex, age and body size on the abundance of their lice at a migratory stopover site, where the falcons' habitat use and behaviour are more homogeneous across sex and age categories than during the breeding season. We sampled Amur Falcons in Nagaland, India at major roosting sites in 2016. We applied generalized linear models (with negative binomial distribution and log-link) to model the abundance of their two most numerous lice (Colpocephalum subzerafae and Degeeriella rufa) using the host age category (juvenile or adult) and wing length, both in interaction with sex, as explanatory variables. The abundance of C. subzerafae was only affected by host age, being nearly four times higher on juveniles than on adults. Juveniles were also more infested with D. rufa than the adults. Additionally, the abundance of the latter species was lower on adult male Falcons as compared to adult females. A juvenile bias in ectoparasite infestations is common in nature, probably due to juveniles being immunologically naïve, more resource-limited and may be inexperienced in body maintenance behaviours like preening and grooming. On the other hand, female-biassed infestations are much rarer than male-biassed infestations. We briefly discuss the possible causes of female-biassed infestations on Amur Falcons reported here, and in the closely related Red-footed Falcon and Lesser Kestrel as reported in the literature.

Sex-dependent changes in the louse abundance of red-footed falcons (Falco vespertinus).

Permanent ectoparasites live in stable environments; thus, their population dynamics are mostly adapted to changes in the host life cycle. We aimed to investigate how static and dynamic traits of red-footed falcons interplay with the dynamics of their louse subpopulations during breeding and how they affect the colonisation of new hosts by lice. We sampled red-footed falcon (Falco vespertinus) nestlings (two breeding seasons) and adults (one breeding season) in southern Hungary. The mean abundance of Colpocephalum subzerafae and Degeeriella rufa lice on the nestlings was modelled with generalized linear mixed models using clutch size and host sex in interaction with wing length. For adults, we used wing length and the number of days after laying the first egg, both in interaction with sex. D. rufa abundances increased with the nestlings' wing length. In one year, this trend was steeper on females. In adult birds, both louse species exhibited higher abundances on females at the beginning, but it decreased subsequently through the breeding season. Contrarily, abundances were constantly low on adult males. Apparently, D. rufa postpones transmission until nestlings develop juvenile plumage and choose the more feathered individual among siblings. The sexual difference in the observed abundance could either be caused by the different plumage, or by the females' preference for less parasitized males. Moreover, females likely have more time to preen during the incubation period, lowering their louse burdens. Thus, sex-biased infestation levels likely arise due to parasite preferences in the nestlings and host behavioural processes in the adult falcons.

Rensch's rule in avian lice: contradictory allometric trends for sexual size dimorphism.

Rensch's rule (RR) postulates that in comparisons across closely related species, male body size relative to female size increases with the average size of the species. This holds true in several vertebrate and also in certain free-living invertebrate taxa. Here, we document the validity of RR in avian lice using three families (Philopteridae, Menoponidae, and Ricinidae). Using published data on the body length of 989 louse species, subspecies, or distinct intraspecific lineages, we applied phylogenetic reduced major axis regression to analyse the body size of females vs. males while accounting for phylogenetic non-independence. Our results indicate that philopterid and menoponid lice follow RR, while ricinids exhibit the opposite pattern. In the case of philopterids and menoponids, we argue that larger-bodied bird species tend to host lice that are both larger in size and more abundant. Thus, sexual selection acting on males makes them relatively larger, and this is stronger than fecundity selection acting on females. Ricinids exhibit converse RR, likely because fecundity selection is stronger in their case.

Biostatistics for Parasitologists - A Primer to Quantitative Parasitology.

The aggregated distributions of host-parasite systems require several different infection parameters to characterize them. We advise readers how to choose infection indices with clear and distinct biological interpretations, and recommend statistical tests to compare them across samples. A user-friendly and free software is available online to overcome technical difficulties.

Armillifer-Infected Snakes Sold at Congolese Bushmeat Markets Represent an Emerging Zoonotic Threat.

African pythons (Pythonidae) and large vipers (Bitis spp.) act as definitive hosts for Armillifer armillatus and Armillifer grandis parasites (Crustacea: Pentastomida) in the Congo Basin. Since the proportion of snakes in bushmeat gradually increases, human pentastomiasis is an emerging zoonotic disease. To substantiate the significance of this threat, we surveyed snakes offered for human consumption at bushmeat markets in the Kole district, Democratic Republic of the Congo, for the presence of adult pentastomids. In Bitis vipers (n = 40), Armillifer spp. infestations exhibited an 87.5% prevalence and 6.0 median intensity. Parasite abundance covaried positively with viper length, but not with body mass. In pythons (n = 13), Armillifer spp. exhibited a 92.3% prevalence and 3.5 median intensity. The positive correlations between parasite abundance and python length or mass were statistically nonsignificant. Ninety-one percent of A. grandis were discovered in vipers and 97% of infected vipers hosted A. grandis, whereas 81% of A. armillatus specimens were found in pythons and 63% of infected pythons hosted A. armillatus. Thus, challenging the widespread notion of strict host specificity, we found 'reversed' infections and even a case of coinfection. In this study, we also gathered information about the snake consumption habits of different tribal cultures in the area. Infective parasite ova likely transmit to humans directly by consumption of uncooked meat, or indirectly through contaminated hands, kitchen tools or washing water.

The evolutionary logic of sepsis.

The recently proposed Microbiome Mutiny Hypothesis posits that members of the human microbiome obtain information about the host individuals' health status and, when host survival is compromised, switch to an intensive exploitation strategy to maximize residual transmission. In animals and humans, sepsis is an acute systemic reaction to microbes invading the normally sterile body compartments. When induced by formerly mutualistic or neutral microbes, possibly in response to declining host health, sepsis appears to fit the 'microbiome mutiny' scenario except for its apparent failure to enhance transmission of the causative organisms. We propose that the ability of certain species of the microbiome to induce sepsis is not a fortuitous side effect of within-host replication, but rather it might, in some cases, be the result of their adaptive evolution. Whenever host health declines, inducing sepsis can be adaptive for those members of the healthy human microbiome that are capable of colonizing the future cadaver and spread by cadaver-borne transmission. We hypothesize that such microbes might exhibit switches along the 'mutualist - lethal pathogen - decomposer - mutualist again' scenario, implicating a previously unsuspected, surprising level of phenotypic plasticity. This hypothesis predicts that those species of the healthy microbiome that are recurring causative agents of sepsis can participate in the decomposition of cadavers, and can be transmitted as soil-borne or water-borne infections. Furthermore, in individual sepsis cases, the same microbial clones that dominate the systemic infection that precipitates sepsis, should also be present in high concentration during decomposition following death: this prediction is testable by molecular fingerprinting in experimentally induced animal models. Sepsis is a leading cause of human death worldwide. If further research confirms that some cases of sepsis indeed involve the 'mutiny' (facultative phenotypic switching) of normal members of the microbiome, then new strategies could be devised to prevent or treat sepsis by interfering with this process.

Do small samples underestimate mean abundance? It depends on what type of bias we consider.

Former authors claimed that, due to parasites' aggregated distribution, small samples underestimate the true population mean abundance. Here we show that this claim is false or true, depending on what is meant by 'underestimate' or, mathematically speaking, how we define 'bias'. The 'how often' and 'on average' views lead to different conclusions because sample mean abundance itself exhibits an aggregated distribution: most often it falls slightly below the true population mean, while sometimes greatly exceeds it. Since the several small negative deviations are compensated by a few greater positive ones, the average of sample means approximates the true population mean.

Size matters for lice on birds: Coevolutionary allometry of host and parasite body size.

Body size is one of the most fundamental characteristics of all organisms. It influences physiology, morphology, behavior, and even interspecific interactions such as those between parasites and their hosts. Host body size influences the magnitude and variability of parasite size according to Harrison's rule (HR: positive relationship between host and parasite body sizes) and Poulin's Increasing Variance Hypothesis (PIVH: positive relationship between host body size and the variability of parasite body size). We analyzed parasite-host body size allometry for 581 species of avian lice (∼15% of known diversity) and their hosts. We applied phylogenetic generalized least squares (PGLS) methods to account for phylogenetic nonindependence controlling for host and parasite phylogenies separately and variance heterogeneity. We tested HR and PIVH for the major families of avian lice (Ricinidae, Menoponidae, Philopteridae), and for distinct ecological guilds within Philopteridae. Our data indicate that most families and guilds of avian lice follow both HR and PIVH; however, ricinids did not follow PIVH and the "body lice" guild of philopterid lice did not follow HR or PIVH. We discuss mathematical and ecological factors that may be responsible for these patterns, and we discuss the potential pervasiveness of these relationships among all parasites on Earth.

Co-infections in Visceral Pentastomiasis, Democratic Republic of the Congo.

Snakeborne Armillifer pentastomiasis is an emerging human parasitic infection in rural tropical areas where snake meat is eaten. After a series of severe ocular A. grandis larval infections and anecdotal abdominal infection in Sankuru District, Democratic Republic of the Congo, during 2014-2015, we systematically investigated possible pentastomid etiology in patients who underwent surgery in the region. Histologic and molecular analyses by established pentastomid 18S rDNA- and newly developed Armillifer-specific cytochrome oxidase PCRs revealed larval pentastomid lesions in 3.7% of patients. Some persons had A. armillatus and A. grandis co-infections. Another pentastomid larva, Raillietiella sp., was molecularly detected in 1 patient who had concomitant A. grandis and A. armillatus infection. The PCRs used were suitable for detecting pentastomid species even in highly necrotic tissues. Phylogenetic analyses of Armillifer cytochrome oxidase genes detected multiple local strains.

Distribution of the myrmecoparasitic fungus Rickia wasmannii (Ascomycota: Laboulbeniales) across colonies, individuals, and body parts of Myrmica scabrinodis.

The ant species Myrmica scabrinodis plays a markedly important ecological role through much of the humid grasslands of Eurasia. It hosts a species-rich community of pathogens and parasites, including Rickia wasmannii, an enigmatic member of entomoparasitic laboulbenialean fungi. This study provides a descriptive ecology of R. wasmannii by characterizing its prevalence and distribution across several hierarchical levels: colonies, individuals, and anatomic body parts. Infections were restricted to a single ant species, M. scabrinodis, and infected colonies occurred predominantly in wet habitats. Infections tended to be highly prevalent within infected colonies, often reaching 100% sample prevalence among workers. Individual infections exhibited an aggregated distribution typical to host-parasite systems. Workers from the aboveground part of nests (presumably older ones acting as foragers) were more infected than those from the belowground part. Fungal thalli could be found all over the body of the hosts, the head and the abdomen being the most infected parts of the body. The fungi's distribution among host body parts statistically differed between low versus high-intensity infections: the initial dominance of the head decreased with advancing infection. These findings may provide baseline data for future comparative or monitoring studies.

Molecular Diagnosis of Abdominal Armillifer grandis Pentastomiasis in the Democratic Republic of Congo.

Pentastomiasis is an emerging snake-borne parasitic zoonosis in the tropics. We describe a molecular and morphological study to diagnose a cluster of asymptomatic abdominal human infections caused by Armillifer grandis. The findings may indicate a silent epidemic in a rural area where severe symptomatic ocular cases with the same parasite species have recently surfaced. Molecular diagnostics are of increasing importance when patient material from remote areas cannot be thoroughly examined locally for logistic reasons.

The microbiome mutiny hypothesis: can our microbiome turn against us when we are old or seriously ill?

BACKGROUND: The symbiotic organisms of the healthy microbiome tend to be harmless or even beneficial for the host; however, some symbionts are able to adjust their virulence in response to external stimuli. Evolutionary theory suggests that optimal virulence might increase if the mortality of the host (from unrelated causes) increases. PRESENTATION OF THE HYPOTHESIS: We hypothesize that microorganisms of the human microbiome may be capable of a coordinated phenotypic switch to higher virulence ("microbiome mutiny") in old or seriously ill people, to optimize their transmission under the conditions of increased background mortality. This proposed virulence shift might contribute to the death of old or seriously ill people even in the absence of apparent disease. TESTING THE HYPOTHESIS: Testable predictions of the hypothesis include increased expression of virulence factors in isolates of the same species of the microbiome obtained from ailing/old versus healthy/young individuals, and the existence of microbial mechanisms to assess the general condition (background mortality) of the host. Such tests are going to be important to distinguish the cases of "microbiome mutiny" from the situation where opportunistic infections or increased effective virulence arise from relaxed immune control in ailing or old individuals in the absence of changes in the symbionts/pathogens. IMPLICATIONS OF THE HYPOTHESIS: Elucidating this potential mechanism might open up new possibilities for the clinical management of age related health issues and critical injuries or disease. Targeted prophylaxis against the microbes capable of virulence shifts could break the harmful feedback loop between deteriorating health and the "mutiny" of the microbiome.

Ocular pentastomiasis in the Democratic Republic of the Congo.

Ocular pentastomiasis is a rare infection caused by the larval stage of pentastomids, an unusual group of crustacean-related parasites. Zoonotic pentastomids have a distinct geographical distribution and utilize reptiles or canids as final hosts. Recently, an increasing number of human abdominal infections have been reported in Africa, where pentastomiasis is an emerging, though severely neglected, tropical disease. Here we describe four ocular infections caused by pentastomids from the Democratic Republic of the Congo. Two cases underwent surgery and an Armillifer grandis infection was detected by morphological and molecular approaches. Thus far, 15 other cases of ocular pentastomiasis have been reported worldwide. Twelve cases were caused by Armillifer sp., recorded almost exclusively in Africa, where such infections occur as a consequence of hunting and consuming snakes, their final hosts. Seven further cases were caused by Linguatula serrata, a cosmopolitan pentastomid whose final hosts are usually canids. Intraocular infections caused permanent visual damage in 69% and a total loss of vision in 31% of reported cases. In contrast, ocular adnexal cases had a benign clinical course. Further research is required to estimate the burden, therapeutic options and pathogenesis of this neglected disease.

A proposal for the classification of biological weapons sensu lato.

Due to historical and legislation reasons, the category of bioweapons is rather poorly defined. Authors often disagree on involving or excluding agents like hormones, psychochemicals, certain plants and animals (such as weeds or pests) or synthetic organisms. Applying a wide definition apparently threatens by eroding the regime of international legislation, while narrow definitions abandon several important issues. Therefore, I propose a category of 'biological weapons sensu lato' (BWsl) that is defined here as any tool of human aggression whose acting principle is based on disciplines of biology including particularly microbiology, epidemiology, medical biology, physiology, psychology, pharmacology and ecology, but excluding those based on inorganic agents. Synthetically produced equivalents (not necessarily exact copies) and mock weapons are also included. This definition does not involve any claim to subject all these weapons to international legislation but serves a purely scholarly purpose. BWsl may be properly categorized on the base of the magnitude of the human population potentially targeted (4 levels: individuals, towns, countries, global) and the biological nature of the weapons' intended effects (4 levels: agricultural-ecological agents, and non-pathogenic, pathogenic, or lethal agents against humans).